Induction of glandular trichomes to control whitefly-transmitted viruses in tomato crops: modulation by the natural enemy Nesidiocoris tenuis

Whitefly-transmitted viruses are one of the biggest threats to tomato growing worldwide. Strategies based on the introgression of resistance traits from wild relatives are promoted to control tomato pests and diseases. Recently, a trichome-based resistance characterizing the wild species Solanum pimpinellifolium was introgressed into a cultivated tomato. An advanced backcross line (BC5S2) exhibiting the presence of acylsugars-associated type IV trichomes, which are lacking in cultivated tomatoes, was effective at controlling whiteflies (Hemiptera: Aleyrodidae) and limiting the spread of whitefly-transmitted viruses. However, at early growth stages, type IV trichomes density and acylsugars production are limited; thus, protection against whiteflies and whitefly-transmitted viruses remains irrelevant. In this work, we demonstrate that young BC5S2 tomato plants feeding-punctured by the zoophytophagous predator Nesidiocoris tenuis (Reuter) (Hemiptera: Miridae) displayed an increase (above 50%) in type IV trichomes density. Acylsugars production was consistently increased in N. tenuis-punctured BC5S2 plants, which was more likely associated with upregulated expression of BCKD-E2 gene related to acylsugars biosynthesis. In addition, the infestation of BC5S2 plants with N. tenuis effectively induced the expression of defensive genes involved in the jasmonic acid signaling pathway, resulting in strong repellence to B. tabaci and attractiveness to N. tenuis. Thus, by pre-plant release of N. tenuis in tomato nurseries carried out in some integrated pest management programs, type IV trichome-expressing plants can be prepared to control whiteflies and whitefly-transmitted viruses at early growth stages. This study emphasizes the advantage of reinforcing constitutive resistance using defense inducers to guarantee robust protection against pests and transmitted viruses.